The future of HIV testing in eastern and southern Africa: Broader scope, targeted services

In this Policy Forum, Anna Grimsrud and colleagues discuss the future of HIV testing in eastern and southern Africa, using insights gleaned from a 2021 expert consultation.

• In eastern and southern Africa (ESA), home to more than half of people living with HIV globally, many countries are close to reaching global targets for HIV treatment and viral suppression, with slower progress towards the global target that 95% of people should know their HIV status. Given this, it is critical to update the approach to HIV testing to reflect changes in the HIV epidemic, the response to it, and to acknowledge ongoing resource constraints.
• An expert consultation series defined this updated approach as a shift to "broader scope, targeted services." Over the next decade, HTS in ESA should implement a status-neutral approach that maintains core testing services to reach the greatest number of people with HIV not on treatment, while broadening the scope to support linkage to appropriate prevention and treatment. It is important that HTS programs use a strategic mix of modalities focused on people most likely to have undiagnosed HIV, those who are not on ART, and people who are more vulnerable to HIV acquisition.
• Ten key themes for the future of HTS were articulated. The most critical are: promote a status-neutral approach to HTS; realize the potential of HIV self-testing (HIVST); prioritize facility-based HTS; reframe retesting among those previously diagnosed but not currently on antiretroviral therapy (ART) as an opportunity; and involve and invest in community leadership and community-led monitoring (CLM) to ensure HTS meets the needs and preferences of clients.

Introduction
In the 40 years since AIDS was first reported, many countries in eastern and southern Africa (ESA), the region most affected by HIV, have made substantial progress towards the global 2025 HIV testing target of 95% of people with HIV being diagnosed [1]. Knowledge of HIV status increased from 5% to 86% in eastern Africa and 9% to 90% in southern Africa between 2000 and 2020. [2]. Concurrently, there was a decrease in the median time to diagnosis (11 and 7.7 years to 2.0 and 1.5 years), HIV positivity (11% and 15% to 2.5% and 5.5%), and the proportion of first-time diagnoses among all positive tests (91% and 87% to 41% and 39%) [2]. While the decrease in time to diagnosis is a remarkable achievement, the decrease in positivity and proportion of first-time diagnoses highlight the need for HTS to evolve to meet the needs of the HIV response. Continuous optimization of effective strategies, innovation, and monitoring are needed to accelerate the decline in HIV incidence.

Defining the future of HIV testing through an expert consultation series
In 2021, International AIDS Society (IAS), the World Health Organization (WHO), and the Bill & Melinda Gates Foundation (BMGF) convened an expert consultation, "The future of HIV testing: Beyond reaching the first 95 in sub-Saharan Africa", to define a vision for HIV testing services (HTS) for the next decade in the context of an evolving epidemic and response. While the consultation title referred to sub-Saharan Africa, the discussion was more specifically focused on high-HIV burden countries in ESA. The expert consultation, a virtual threepart series, included 78 stakeholders who were invited based on their experience in HTS and who live or work in 11 ESA countries. Sessions 1 ("Past success, present priorities and future opportunities") and 2 ("The different, and sometimes competing, roles of HIV testing") included presentations and discussions. Session 3 was a response to the first 2 sessions and involved breakout groups to facilitate inputs from all participants. The consultation agenda is available as S1 Appendix and details of the participants in S2 Appendix. Participants articulated a vision of the future of HIV testing in the region and 10 supporting key themes (Table 1). In this paper, we present this vision along with key themes.

A vision for HIV testing services in ESA for the next decade: Broader scope, targeted services
Our vision for HTS in ESA for the next decade involves an important shift, where the scope of HTS is broadened towards "status-neutral" testing that actively supports linkage to and engagement in prevention or treatment programs [30]. The shift will increase HTS volume Understand and accept that a subset of people who know they have HIV will attend HTS for retesting.
Use HTS as an opportunity for those not successfully linked to ART or who have disengaged from ART to (re)start treatment.
• Recognizing that retesting and "diagnosis confirmation" is a legitimate and effective linkage strategy for ART engagement • Accepting and productively engaging with individuals who use HTS as a means of returning to ART care [14] • Strengthening health information systems to identify individuals previously diagnosed who are re-engaging in ART care through retesting • Presuming that those testing positive are newly diagnosed • Considering retesting (apart from verification testing) among those who were previously diagnosed as always wasteful • Not addressing underlying reasons for retesting among those previously diagnosed [15] • Reviewing routine data to see the proportion of those initiating treatment who are non-naïve such as in South Africa [16] • Prior exposure to ART among adult patients presenting for HIV treatment initiation or re-initiation in sub-Saharan Africa: a systematic review [14] 6. Involve communities and invest in CLM Increase community engagement through leadership and participation in HTS design, monitoring and adaptation of HTS to ensure services meet the needs and preferences of people using the service and that service delivery is adapted to reach those least likely to access care • Supporting HIVST via digital platforms to expand reach and uptake [23] • Using virtual interventions including social media, live chats, short message services, and apps, to bolster HTS [24] (Continued ) while also targeting services towards the people who are most likely to be at risk of acquiring HIV. It also emphasizes continual country-led and evidence-based adaptation of HTS to an evolving HIV epidemic, with a commitment to human rights and community engagement.
Metrics of success will extend beyond HIV positivity. Countries could collectively adapt this vision to revise national HTS policies, program planning, and implementation, including related targets and indicators.

Background
Knowledge of HIV status is only one aspect of HTS. To maximize individual and public health benefits, it is critically important that HTS actively links individuals to prevention and treatment services and support them to remain engaged in care; those who test negative need to be linked, with support, to prevention services. Previously, when there was limited access to treatment and prevention interventions, HTS emphasized "know your status." As treatment became more available, there was increased emphasis on the HIV positivity rate and rapid linkage to ART to achieve viral load suppression, to improve the individual's health, and to decrease HIV transmission to others. HTS was integral to a "treat all" approach that focused on case finding and linkage to treatment services.

Importance to the future of HIV testing
Biomedical prevention options continue to expand beyond the cornerstones of condoms, voluntary medical male circumcision (VMMC), and prevention services for key populations, to include an increasing range of pre-exposure prophylaxis (PrEP) options. A parallel shift in HTS delivery-to status-neutral testing-is required [30]. This approach is intended to broaden HTS beyond case-finding, to serve populations at ongoing risk of HIV acquisition by Provide population-and provider-level HIV prevention and treatment literacy, including the preventive benefits of ART ("U = U" messaging) [25] • Recognizing that population-level stigma reduction remains critical to reaching those underserved [26] • Investing in multi-stakeholder buy-in and delivery of population-level countryspecific HIV epidemic literacy with a focus on locally adapted U = U related education and messaging [27] • expanding access to HTS and actively linking clients to prevention services (Fig 1) [31]. It also supports early identification of new cases through partner, index, and social-network testing, and linkage to and support for sustained engagement in treatment services for those who test positive [32]. Shifting HTS to a status-neutral approach requires buy-in from stakeholders, adequate funding, and revised targets and metrics including new HTS indicators for linkage to prevention and retesting coverage as defined in the WHO 2022 guidelines on person-centered HIV strategic information [33]. Increased referral from HTS should result in increased uptake and more effective engagement in prevention services, requiring additional resources. Measures of HTS success should include both prevention (condom programming, PrEP, needle and syringe programming (NSP), opioid agonist maintenance therapy (OAMT), VMMC, and PMTCT) and treatment (ART initiations, re-engagement in ART).
Broadening the scope of HTS will increase HTS volume and therefore require strategic financing approaches. Global stakeholders will need to prioritize and facilitate reduced costs for professional use HIV rapid test kits while continuing to reduce HIVST costs through market diversification and development, promotion of pooled purchasing power, support for country tender negotiation processes, and direct manufacturer price negotiation strategies. The recent announcement of US$ 1 HIV self-tests is one example of innovation in the funding [31]. Legend: HIV testing services result in an action-either the red arrows for someone who is living with HIV or the black arrows for the person who tests HIV negative. HIV testing services are therefore status-neutral, with benefits and an action regardless of the test outcomes. The person on the left receives HIV testing services. If they test positive for HIV, they follow the red arrow up and are linked to and initiated on ART. They continue to follow the red arrows and are engaged in HIV care and achieve viral suppression. They may interrupt treatment and need to be re-engaged in care. By achieving and sustaining viral suppression, they have zero risk of transmitting HIV and reduced morbidity and mortality. If the person on the left receives HIV testing services and tests negative for HIV, they will follow the black arrows along the bottom. If they are at ongoing risk of HIV exposure, they should have their risk assessed by a provider. They may need to be provided with PrEP and supported to use PrEP effectively to have negligible risk of HIV acquisition. While on PrEP, they should also be provided with frequent HIV and STI testing. space [30]. Maximizing the use of dual HIV/syphilis rapid testing is another potentially costeffective strategy in antenatal care (ANC) settings [34].

Background
HIVST is an important tool for increasing access to and uptake of HTS. HIVST enables people to test when and where they prefer and to initiate linkage and engagement in treatment and/or prevention services. It is a highly acceptable and effective way to reach people who do not test through other HTS delivery options or who need more frequent testing due to ongoing HIV risk [35]. Since 2017, the number of countries with policies supportive of HIVST and where HIVST kits are distributed has increased significantly [36], but there are still many countries where HIVST is not supported. More work on national policy adoption and resources necessary to realize the full potential of HIVST is needed. Tracking of each HIVST kit adds complexity to the process, particularly with secondary distribution models, and compromises anonymity. It may be more effective to monitor kit distribution through public sector tracking models or private sector sales volumes, identifying the groups being reached via self-report during population-based surveys, and using routine HTS data to triangulate HIVST impact.

Importance to the future of HIV testing
HIVST is not an alternative to conventional testing but an additional testing option for individuals who have not tested or who are unlikely to test through other approaches [37]. HIVST can play a critical role within HIV testing modalities-including as a highly sensitive "screening-in tool" at health facilities. This option can reduce pressure on the health workforce while increasing testing opportunities through other entry points such as outpatient [38], contraception, and/or sexually transmitted infection (STI) services. HIVST also increases communityand workplace-based access for specific populations including adolescents, key populations, and men [39]. Social and virtual networks remain underutilized for distribution of HIVST kits and may benefit from improved messaging for specific populations about the benefits of HIVST. HIVST is also useful for increasing uptake of PrEP by reducing the need to return to health facilities for HTS and thus supporting differentiated PrEP service delivery models [40]. Ultimately, HIVST could play an important role in rebranding HIV testing as a regular part of self-care for certain populations and geographical settings, similar to the role of self-testing for Coronavirus Disease 2019 (COVID-19).

Background
Quality facility-based HTS is the backbone of an HTS program. However, with declining resources for testing and a focus on the positivity rate, countries have been pushed to reduce lower-"yield" HIV testing approaches, trading case-finding volume for testing positivity. Outpatient departments have seen the largest reductions in HIV testing. COVID-19 provided a real-world case study of the impact of large reductions in delivery of facility-based HTS: In 2020, fewer people, particularly men, were tested for HIV, resulting in fewer ART initiations [41][42][43]. Reducing facility-based HTS may also reduce opportunities to identity clients with advanced HIV disease who present only when acutely ill and who will benefit from the earliest possible diagnosis and treatment.
The diffuse nature of HIV transmission in ESA is characterized by a large number of people at a low risk of acquiring HIV, making provider-initiated testing and counseling (PITC) particularly important [44]. Recent analysis highlights transmission in small, diffuse clusters driven by "many who transmit to a few, rather than by a few who transmit to many" [45]. Further, more than three-quarters of new HIV infections are acquired from people who have been living with HIV for more than a year [46], counter to a previous assumption that identification of new infections to prevent transmission should be the primary focus of prevention programming.

Importance to the future of HIV testing
Facility-based HTS is not requiring testing of every person but offering HTS to those presenting to health services with conditions or preventive health needs that may indicate a need for HTS. There is no evidence that the "worried well" represent a significant proportion of people seeking testing in facilities, and screening tools used to reduce HIV testing volumes within health facilities for adults are not often validated and have been shown to miss people who would have been otherwise tested [47]. Rather than limiting the routine offer of testing, a more evidence-based approach would be to align the volume of clinic-based HIV testing offered across clinical services (e.g., outpatient, ANC, TB, or STI) informed by epidemiological and program data [11]. In much of ESA, testing in ANC, TB, STI, and contraception outpatient services should be prioritized. The success of these efforts could then be measured with treatment-adjusted prevalence and absolute numbers of positive diagnoses, rather than solely casefinding yield [10,48].

Background
Significant progress on knowledge of HIV status remains variable by region, within countries, and across populations [49]. Adolescent girls and young women have greater access to HTS and ART services due to more frequent engagement with sexual and reproductive health services (especially ANC) compared to adolescent boys and young men. In ESA, only 65% of youth living with HIV (15 to 24 years) know their status (65%), and men aged 35 to 49 years with HIV account for the highest number unaware of their status, with an estimated 701,000 men undiagnosed [2]. Only 66% of children in ESA under 15 years of age know their HIV status compared to 91% of people 15 years and older [1]. Key populations and their partners accounted for 46% of new infections in ESA in 2021 [1] and are a critically undertested population. All of these populations would benefit from improved access to HTS.

Importance to the future of HIV testing
Despite global guidance recommending implementation of specific evidence-based testing approaches to effectively target and diagnose untested populations [50], investment has been insufficient to scale these approaches. As with facility-based testing, implementation of a mix of community-based models requires adaptation to local needs and resources. Investment should cover commodities and programmatic needs including participation of key populations in HTS implementation. Empowerment of underserved populations requires improved engagement [51]and mobilization of social networks, index cases, and community actors to provide HIV testing, including distribution of HIVST kits [52].
Virtual platforms, index-and social-network testing and other specific population-targeted, community-based testing strategies are likely to increase uptake of testing among key populations, men, and children [53]. Programs need to determine the resources needed to adequately support targeted community-based HTS without depleting facility-based resources.

Background
It is increasingly recognized that the HIV care continuum is cyclical [54]. Some people with an HIV diagnosis test multiple times, seeking confirmation while delaying (or never) linking to treatment; others retest after disengagement from treatment as a route to re-engagement [55]. Both delayed linkage and disengagement from ART can have negative individual and public health consequences. Among those with HIV who know their status, new data suggest an increasing proportion of people testing positive have previously received an HIV diagnosis [14] For example, in South Africa, half of those testing positive had previously received an HIV diagnosis [56], with only half of them self-reporting prior knowledge of their status.

Importance to the future of HIV testing
HTS providers may benefit from a reorientation to their vital role in linking and relinking individuals living with HIV to treatment. HTS providers can provide critical support by retesting individuals who are struggling to accept their diagnosis and start ART. In parallel, clients should receive counseling on the benefits of ART for their own health and on the critical value of viral suppression in protecting their sexual partners: increasing knowledge of U = U (undetectable is equal to untransmittable) can reduce self-stigma and anxiety [57]. HTS providers should also accept and enable retesting as a means to facilitate re-engagement in treatment services. Doing so may help facilitate reentry, especially for people who may fear judgmental health providers or who experience a sense of failure associated with not staying on ART [58]. As the epidemic continues to mature, people cycling in and out of care will contribute an increasingly large fraction of transmission [45]. Providing HTS services to those previously diagnosed should be seen as an opportunity, not a burden.

Background
It is important that people who use HIV services participate in the design, monitoring, and adaptation of services. Increased agency through community-led monitoring (CLM) also supports participation and health system accountability and responsiveness. Effective CLM depends on continuous data collection, analysis, and utilization by clients, health-service providers, and national stakeholders [17].

Importance to the future of HIV testing
Community participation fosters person-centered services. Communities need to be actively engaged to inform policy, implementation guidance, and demand creation-all of which can be bolstered with better utilization of CLM data. People who use services have important insights into HTS delivery adaptations necessary to reach the unreached. CLM metrics could include HTS quality indicators for both first-time testers and retesters, and for those using HTS to re-engage in prevention and/or treatment services. Increased investment in CLMfinancial, technical, and political-can ensure that HTS meet the needs and preferences of people using services.
Details of 4 final themes are outlined in Table 1. In brief, HTS will benefit from being integrated and person-centered with primary healthcare services across a range of health conditions [19]. There are opportunities with virtual interventions and digital tools to bolster the provision of HTS, including but not limited to expanding access to HIVST [24]. The vision of status-neutral testing will benefit from improved HIV health literacy including around U = U messaging [25], and finally, the strategic mix of differentiated HTS will require regular reviews and updates that are data driven.

Conclusion
Defining a shared vision for the next decade of HIV testing services in ESA is an essential first step to implementing more efficient, effective, and acceptable testing programs that are required to reach and maintain the 2025 UNAIDS prevention and treatment targets. The next step is collaborating with communities, Ministries of Health, health workers, funders, normative agencies, and implementing partners to translate this vision into practice. Successful implementation of this vision will require alignment with global funders and increased autonomy for ministries of health to implement context-driven HTS programming. A shift towards a status-neutral approach to HTS implementation is appropriate in the setting of ESA where "many are transmitting to a few" [45] making linkage and engagement to both prevention and treatment critical. Topics not sufficiently covered by the consultation that need further engagement include how to finance a status-neutral approach to HTS and determining the themes that may be most relevant for other regions. In addition, it is important to recognize that even the countries in ESA are heterogenous; as their epidemics and responses evolve, program data and context-specific studies will be needed to adjust and refine the implementation of the proposed broader, more targeted approach to HTS that will advance both HIV treatment and prevention objectives.